A collective mechanism for phase variation in biofilms

Understanding how microbes gather into biofilm communities and maintain diversity remains one of the central questions of microbiology, requiring an understanding of microbes as communal rather then individual organisms. Phase variation plays an integral role in the formation of diverse phenotypes within biofilms. We propose a collective mechanism for phase variation based on gene transfer agents, and apply the theory to predict the population structure and growth dynamics of a biofilm. Our results describe quantitatively recent experiments, with the only adjustable parameter being the rate of intercellular horizontal gene transfer. Our approach derives from a more general picture for the emergence of cooperation between microbes.

[1]  A. L. Koch Unidirectional Movement of Flares of Cells of Myxococcus xanthus , 2006, Critical reviews in microbiology.

[2]  J. Hacker,et al.  A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256 , 1999, Molecular microbiology.

[3]  D. Grogan Exchange of genetic markers at extremely high temperatures in the archaeon Sulfolobus acidocaldarius , 1996, Journal of bacteriology.

[4]  J. Shapiro Thinking about bacterial populations as multicellular organisms. , 1998, Annual review of microbiology.

[5]  C. Woese A New Biology for a New Century , 2004, Microbiology and Molecular Biology Reviews.

[6]  S. Rice,et al.  Phenotypic Diversification and Adaptation of Serratia marcescens MG1 Biofilm-Derived Morphotypes , 2006, Journal of bacteriology.

[7]  A. Richardson,et al.  Natural transformation and phase variation modulation in Neisseria meningitidis , 2004, Molecular microbiology.

[8]  M. Simon,et al.  Phase variation in Salmonella: genetic analysis of a recombinational switch. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Dale Kaiser,et al.  Coupling cell movement to multicellular development in myxobacteria , 2003, Nature Reviews Microbiology.

[10]  H. Seifert,et al.  DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae , 1988, Nature.

[11]  Matthew R. Parsek,et al.  Characterization of Colony Morphology Variants Isolated from Pseudomonas aeruginosa Biofilms , 2005, Applied and Environmental Microbiology.

[12]  Laura S. Frost,et al.  Mobile genetic elements: the agents of open source evolution , 2005, Nature Reviews Microbiology.

[13]  Ariel B. Lindner,et al.  Neurokinin 1 Receptor Antagonism as a Possible Therapy for Alcoholism , 2008, Science.

[14]  D. Grogan,et al.  Conjugational Genetic Exchange in the Hyperthermophilic Archaeon Sulfolobus acidocaldarius: Intragenic Recombination with Minimal Dependence on Marker Separation , 2005, Journal of bacteriology.

[15]  Christopher M Thomas,et al.  Mechanisms of, and Barriers to, Horizontal Gene Transfer between Bacteria , 2005, Nature Reviews Microbiology.

[16]  Richard Moxon,et al.  Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. , 2006, Annual review of genetics.

[17]  T. Meyer,et al.  Reassortment of pilin genes in Neisseria gonorrhoeae occurs by two distinct mechanisms , 1989, Nature.

[18]  Paul Stoodley,et al.  Bacterial biofilms: from the Natural environment to infectious diseases , 2004, Nature Reviews Microbiology.

[19]  S. Kjelleberg,et al.  Ecological Advantages of Autolysis during the Development and Dispersal of Pseudoalteromonas tunicata Biofilms , 2006, Applied and Environmental Microbiology.

[20]  M. Schaller,et al.  Phage release from biofilm and planktonic Staphylococcus aureus cells. , 2005, FEMS microbiology letters.

[21]  J. Costerton,et al.  Microbial Biofilms , 2011 .

[22]  Blaise R. Boles,et al.  Self-generated diversity produces "insurance effects" in biofilm communities. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Townsend,et al.  Horizontal gene transfer, genome innovation and evolution , 2005, Nature Reviews Microbiology.

[24]  J. Costerton,et al.  Biofilms as complex differentiated communities. , 2002, Annual review of microbiology.

[25]  E. Delong,et al.  Environmental diversity of bacteria and archaea. , 2001, Systematic biology.

[26]  A. Richardson,et al.  Mismatch repair and the regulation of phase variation in Neisseria meningitidis , 2001, Molecular microbiology.

[27]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

[28]  E. Cox,et al.  Population Fitness and the Regulation of Escherichia coli Genes by Bacterial Viruses , 2005, PLoS biology.

[29]  M. Deem,et al.  Phase diagrams of quasispecies theory with recombination and horizontal gene transfer. , 2006, Physical review letters.

[30]  S. Kjelleberg,et al.  Bacteriophage and Phenotypic Variation in Pseudomonas aeruginosa Biofilm Development , 2004, Journal of bacteriology.

[31]  A. Gintsburg,et al.  Formation of biofilms as an example of the social behavior of bacteria , 2006, Microbiology.

[32]  M. W. van der Woude,et al.  Phase and Antigenic Variation in Bacteria , 2004, Clinical Microbiology Reviews.

[33]  R. Kolter,et al.  Multicellularity and Biofilms , 2004 .

[34]  R. Kolter,et al.  Microbial sciences: The superficial life of microbes , 2006, Nature.

[35]  M. W. van der Woude Re-examining the role and random nature of phase variation. , 2006, FEMS microbiology letters.

[36]  N. Goldenfeld,et al.  Global divergence of microbial genome sequences mediated by propagating fronts. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  S. Bergström,et al.  Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. , 1987, Genetics.

[38]  Philip Hugenholtz,et al.  Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity , 1998, Journal of bacteriology.

[39]  T. Jahn,et al.  Movement and locomotion of microorganisms. , 1965, Annual review of microbiology.

[40]  K. Verstrepen,et al.  Timescales of Genetic and Epigenetic Inheritance , 2007, Cell.

[41]  Stefan Wuertz,et al.  Studying plasmid horizontal transfer in situ: a critical review , 2005, Nature Reviews Microbiology.

[42]  Jeff Smith The social evolution of bacterial pathogenesis , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[43]  I. Henderson,et al.  Molecular switches — the ON and OFF of bacterial phase variation , 1999, Molecular microbiology.

[44]  M. Simon,et al.  DNA sequence adjacent to flagellar genes and evolution of flagellar-phase variation , 1983, Journal of bacteriology.